Abstract
Flavonoids and hydroxycinnamic acid derivatives, which are located in the upper epidermis of plants, are well known to screen ultraviolet radiation, thus protecting the underlying tissue from these harmful wavelengths. Both classes of secondary products complement each other over the UV spectral region according to their absorption spectra: flavonoids are most efficient as UV-A attenuators while hydroxycinnamates (HCAs) screen well within the UV-B region. Analysis of epidermal transmittance revealed a substantial UV-A screen in Helianthus annuus L. cv. Peredovick. Identifying responsible pigments by HPLC-MS, we found surprisingly low amounts of flavonoids but dominant abundance of the HCA derivatives chlorogenic and di-caffeoyl quinic acid. Both display low UV-A absorbance and thus, should contribute only a little to UV-A protection. However, growth at high light led to a decrease of epidermal transmittance at 366 nm of up to 90%. Underpinning the screening role, HCA autofluorescence microscopy revealed storage to occur predominantly in vacuoles of the upper epidermis. UV-A treatment in the absence of D1-repair resulted in photosystem II inactivation proportional to epidermal UV-A transmittance. Our findings suggest that UV-A protection can be achieved solely with HCAs, apparently through accumulation of high amounts of these compounds.
Similar content being viewed by others
References
Y. Jiang, M. Rabbi, M. Kim, C. Ke, W. Lee, R. L. Clark, et al., UVA generates pyrimidine dimers in DNA directly, Biophys.J., 2009, 96, 1151–1158.
I. Vass, E. Turcsányi, E. Touloupakis, D. Ghanotakis and V. Petrouleas, The mechanism of UV-A radiation-induced inhibition of photosystem II electron transport studied by EPR and chlorophyll fluorescence, Biochemistry, 2002, 41, 10200–10208.
E. Turcsányi and I. Vass, Inhibition of photosynthetic electron transport by UV-A radiation targets the photosystem II complex, Photochem. Photobiol., 2000, 72, 513–520.
U.S. Department, of Energy (DOE)/NREL/ALLIANCE. ASTM G173-03 Reference Spectra Derived from SMARTS v. 2.9.2 [Internet]. Available from: https://www.nrel.gov/grid/solar-resource/spectra-am1.5.html.
D. Verdaguer, M. A. K. Jansen, L. Llorens, L. O. Morales and S. Neugart, UV-A radiation effects on higher plants: Exploring the known unknown, Plant Sci., 2017, 255, 72–81.
M. Hakala, Photoinhibition of manganese enzymes: insights into the mechanism of photosystem II photoinhibition, J. Exp. Bot., 2006, 57, 1809–1816.
M. Hakala, I. Tuominen, M. Keränen, T. Tyystjärvi and E. Tyystjärvi, Evidence for the role of the oxygen-evolving manganese complex in photoinhibition of photosystem II, Biochim. Biophys. Acta, 2005, 1706, 68–80.
S. Takahashi, S. E. Milward, W. Yamori, J. R. Evans, W. Hillier and M. R. Badger, The solar action spectrum of photosystem II damage, Plant Physiol., 2010, 153, 988–993.
P. Sarvikas, M. Hakala, E. Pätsikkä, T. Tyystjärvi and E. Tyystjärvi, Action spectrum of photoinhibition in leaves of wild type and npq1–2 and npq4-1 mutants of Arabidopsis thaliana, Plant Cell Physiol., 2006, 47, 391–400.
L. W. Jones and B. Kok, Photoinhibition of chloroplast reactions. I. Kinetics and action spectra, Plant Physiol., 1966, 41, 1037–1043.
T. A. Day, T. C. Vogelmann and E. H. DeLucia, Are some plant life forms more effective than others in screening out ultraviolet-B radiation?, Oecologia, 1992, 92, 513–519.
C. S. Cockell, Ultraviolet radiation, evolution and the π-electron system, Biol. J. Linn. Soc., 1998, 63, 449–457.
K. G. Ryan, E. E. Swinny, K. R. Markham and C. Winefield, Flavonoid gene expression and UV photoprotection in transgenic and mutant Petunia leaves, Phytochemistry, 2002, 59, 23–32.
L. G. Landry, C. Chapple and R. L. Last, Arabidopsis mutants lacking phenolic sunscreens exhibit enhanced ultraviolet-B injury and oxidative damage, Plant Physiol., 1995, 109, 1159–1166.
R. Lois and B. B. Buchanan, Severe sensitivity to ultraviolet radiation in an Arabidopsis mutant deficient in flavonoid accumulation: II. Mechanisms of UV-resistance in Arabidopsis, Planta, 1994, 194, 504–509.
J. Li, T. M. Ou-Lee, R. Raba, R. G. Amundson and R. L. Last, Arabidopsis flavonoid mutants are hypersensitive to UV-B irradiation, Plant Cell, 1993, 5, 171–179.
G. Agati and M. Tattini, Multiple functional roles of flavonoids in photoprotection, New Phytol., 2010, 186, 786–793.
M. Tattini, C. Galardi, P. Pinelli, R. Massai, D. Remorini and G. Agati, Differential accumulation of flavonoids and hydroxycinnamates in leaves of Ligustrum vulgare under excess light and drought stress, New Phytol., 2004, 163, 547–561.
G. Agati, C. Brunetti, M. Di Ferdinando, F. Ferrini, S. Pollastri and M. Tattini, Functional roles of flavonoids in photoprotection: New evidence, lessons from the past, Plant Physiol. Biochem., 2013, 72, 35–45.
P. Mølgaard and H. Ravn, Evolutionary aspects of caffeoyl ester distribution in dicotyledons, Phytochemistry, 1988, 27, 2411–2421.
T. Okuda, T. Yoshida, T. Hatano, M. Iwasaki, M. Kubo, T. Orime, et al., Hydrolysable tannins as chemotaxonomic markers in the rosaceae, Phytochemistry, 1992, 31, 3091–3096.
C. Clé, L. M. Hill, R. Niggeweg, C. R. Martin, Y. Guisez, E. Prinsen, et al., Modulation of chlorogenic acid biosynthesis in Solanum lycopersicum; consequences for phenolic accumulation and UV-tolerance, Phytochemistry, 2008, 69, 2149–2156.
L. Mondolot-Cosson, C. Andary, G.-H. Dai and J.-L. Roussel, Histolocalisation de substances phénoliques intervenant lors d’interactions plante-pathogène chez le tournesol et la vigne, Acta Bot. Gallica, 1997, 144, 353–362.
D. Saftić-Panković, S. Veljović-Jovanović, M. Pucarević, N. Radovanović and A. Mijić, Phenolic compounds and peroxidases in sunflower near-isogenic lines after downy mildew infection, Helia, 2006, 29, 33–42.
L. H. Rieseberg, D. E. Soltis and D. Arnold, Variation and localization of flavonoid aglycones in Helianthus annuus (Compositae), Am. J. Bot., 1987, 74, 224–233.
O. Zsiros, S. I. Allakhverdiev, S. Higashi, M. Watanabe, Y. Nishiyama and N. Murata, Very strong UV-A light temporally separates the photoinhibition of photosystem II into light-induced inactivation and repair, Biochim. Biophys. Acta, 2006, 1757, 123–129.
G. Navarra, M. Moschetti, V. Guarrasi, M. R. Mangione, V. Militello and M. Leone, Simultaneous determination of caffeine and chlorogenic acids in green coffee by UV/Vis spectroscopy, J. Chem., 2017.
S. C. Grace, B. A. Logan and W. W. Adams, Seasonal differences in foliar content of chlorogenic acid, a phenylpropanoid antioxidant, in Mahonia repens, Plant, Cell Environ., 1998, 21, 513–521.
F. Pescheck, H. Campen, L. Nichelmann and W. Bilger, Relative sensitivity of DNA and photosystem II in Ulva intestinalis (Chlorophyta) under natural solar irradiation, Mar. Ecol.: Prog. Ser., 2016, 555, 95–107.
W. Bilger, T. Johnsen and U. Schreiber, UV-excited chlorophyll fluorescence as a tool for the assessment of UV-protection by the epidermis of plants, J. Exp. Bot., 2001, 52, 2007–2014.
L. Nichelmann, M. Schulze, W. B. Herppich and W. Bilger, A simple indicator for non-destructive estimation of the violaxanthin cycle pigment content in leaves, Photosynth. Res., 2016, 128, 183–193.
L. Nichelmann and W. Bilger, Quantification of light screening by anthocyanins in leaves of Berberis thunbergii, Planta, 2017, 246, 1069–1082.
B. Harbaum, E. M. Hubbermann, Z. Zhu and K. Schwarz, Free and bound phenolic compounds in leaves of pak choi (Brassica campestris L. ssp. chinensis var. communis) and Chinese leaf mustard (Brassica juncea Coss), Food Chem., 2008, 110, 838–846.
A. Oertel, A. Matros, A. Hartmann, P. Arapitsas, K. J. Dehmer, S. Martens, et al., Metabolite profiling of red and blue potatoes revealed cultivar and tissue specific patterns for anthocyanins and other polyphenols, Planta, 2017, 246, 281–297.
D. Brauch, A. Porzel, E. Schumann, K. Pillen and H.-P. Mock, Changes in isovitexin-O-glycosylation during the development of young barley plants, Phytochemistry, 2018, 148, 11–20.
M. Lang, F. Stober and H. K. Lichtenthaler, Fluorescence emission spectra of plant leaves and plant constituents, Radiat. Environ. Biophys., 1991, 30, 333–347.
J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, et al., Fiji: an open-source platform for biological-image analysis, Nat. Methods, 2012, 9, 676–682.
K. M. Bachmann, V. Ebbert, W. W. Adams III, A. S. Verhoeven, B. A. Logan and B. Demmig-Adams, Effects of lincomycin on PSII efficiency, non-photochemical quenching, D1 protein and xanthophyll cycle during photoinhibition and recovery, Funct. Plant Biol., 2004, 31, 803–813.
J. L. Willems, M. M. Khamis, W. Mohammed Saeid, R. W. Purves, G. Katselis, N. H. Low, et al., Analysis of a series of chlorogenic acid isomers using differential ion mobility and tandem mass spectrometry, Anal. Chim. Acta, 2016, 933, 164–174.
P. Miketova, K. H. Schram, J. Whitney, E. H. Kearns and B. N. Timmermann, Mass spectrometry of 3,5- and 4,5-dicaffeoylquinic acids and selected derivatives, J. Mass Spectrom., 1999, 34, 1240–1252.
L. Mondolot, P. La Fisca, B. Buatois, E. Talansier, A. De Kochko and C. Campa, Evolution in caffeoylquinic acid content and histolocalization during Coffea canephora leaf development, Ann. Bot., 2006, 98, 33–40.
R. del Moral, On the variability of chlorogenic acid concentration, Oecologia, 1972, 9, 289–300.
T. Iwashina, The structure and distribution of the flavonoids in plants, J. Plant Res., 2000, 113, 287–299.
B. Bohm, Chapter Three - Occurrence and distribution of flavonoids, in, Introduction to flavonoids, Harwood Academic Publishers, Amsterdam, 1998, pp. 117–173.
J. Harborne, Chapter two - Phenolic compounds, in, Phytochemical methods: A guide to modern techniques of plant analysis, Chapman and Hall Ltd, London, 1973, pp. 33–88.
J. B. Harborne and D. M. Smith, Anthochlors and other flavonoids as honey guides in the compositae, Biochem. Syst. Ecol., 1978, 6, 287–291.
C. Sando, Anthocyanin formation in Helianthus annuus, J. Biol. Chem., 1925, 71–74.
C. Rice-Evans, N. Miller and G. Paganga, Antioxidant properties of phenolic compounds, Trends Plant Sci., 1997, 2, 152–159.
R. Niggeweg, A. J. Michael and C. Martin, Engineering plants with increased levels of the antioxidant chlorogenic acid, Nat. Biotechnol., 2004, 22, 746–754.
J. J. Sheahan, Sinapate esters provide greater UV-B attenuation than flavonoids in Arabidopsis thaliana (Brassicaceae), Am. J. Bot., 1996, 679–686.
R. D. Hartley and P. J. Harris, Phenolic constituents of the cell walls of dicotyledons, Biochem. Syst. Ecol., 1981, 9, 189–203.
P. J. Harris and R. D. Hartley, Phenolic constituents of the cell walls of monocotyledons, Biochem. Syst. Ecol., 1980, 8, 153–160.
C. A. Kolb, U. Schreiber, R. Gademann and E. E. Pfündel, UV-A screening in plants determined using a new portable fluorimeter, Photosynthetica, 2005, 43, 371–377.
C. A. Kolb, M. A. Käser, J. Kopecky, G. Zotz, M. Riederer and E. E. Pfundel, Effects of natural intensities of visible and ultraviolet radiation on epidermal ultraviolet screening and photosynthesis in grape leaves, Plant Physiol., 2001, 127, 863–875.
T. A. Day, G. Martin and T. C. Vogelmann, Penetration of UV-B radiation in foliage: evidence that the epidermis behaves as a non-uniform filter, Plant, Cell Environ., 1993, 16, 735–741.
G. Karabourniotis, Epicuticular phenolics over guard cells: Exploitation for in situ stomatal counting by fluorescence microscopy and combined image analysis, Ann. Bot., 2001, 87, 631–639.
G. Liakopoulos, Analysis of epicuticular phenolics of Prunus persica and Olea europaea leaves: Evidence for the chemical origin of the UV-induced blue fluorescence of stomata, Ann. Bot., 2001, 87, 641–648.
R. G. Riley and P. E. Kolattukudy, Evidence for covalently attached p-coumaric acid and ferulic acid in cutins and suberins, Plant Physiol., 1975, 56, 650–654.
P. Krauss, C. Markstädter and M. Riederer, Attenuation of UV radiation by plant cuticles from woody species, Plant, Cell Environ., 1997, 20, 1079–1085.
S. S. Thayer and O. Björkman, Leaf Xanthophyll content and composition in sun and shade determined by HPLC, Photosynth. Res., 1990, 23, 331–343.
F. Pescheck and W. Bilger, High impact of seasonal temperature changes on acclimation of photoprotection and radiation-induced damage in field grown Arabidopsis thaliana, Plant Physiol. Biochem., 2019, 134, 129–136.
P. Burchard, W. Bilger and G. Weissenböck, Contribution of hydroxycinnamates and flavonoids to epidermal shielding of UV-A and UV-B radiation in developing rye primary leaves as assessed by ultraviolet-induced chlorophyll fluorescence measurements, Plant, Cell Environ., 2000, 23, 1373–1380.
E. E. Pfündel, N. Ben Ghozlen, S. Meyer and Z. G. Cerovic, Investigating UV screening in leaves by two different types of portable UV fluorimeters reveals in vivo screening by anthocyanins and carotenoids, Photosynth, Res., 2007, 93, 205–221.
P. Jahns and A. R. Holzwarth, The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II, Biochim. Biophys. Acta, Bioenerg., 2012, 1817, 182–193.
S. I. Allakhverdiev and N. Murata, Environmental stress inhibits the synthesis de novo of proteins involved in the photodamage–repair cycle of Photosystem II in Synechocystis sp. PCC 6803, Biochim. Biophys. Acta, 2004, 1657, 23–32.
C. S. Cockell and J. Knowland, Ultraviolet radiation screening compounds, Biol. Rev. Cambridge Philos. Soc., 1999, 74, 311–345.
Author information
Authors and Affiliations
Corresponding author
Additional information
Electronic supplementary information (ESI) available. See DOI: 10.1039/c8pp00440d
Rights and permissions
About this article
Cite this article
Stelzner, J., Roemhild, R., Garibay-Hernández, A. et al. Hydroxycinnamic acids in sunflower leaves serve as UV-A screening pigments. Photochem Photobiol Sci 18, 1649–1659 (2019). https://doi.org/10.1039/c8pp00440d
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1039/c8pp00440d